University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln USDA National Wildlife Research Center - Staff U.S. Department of Agriculture: Animal and Publications Plant Health Inspection Service 2019 Carrion Availability in Space and Time Marcos Moleón Nuria Selva David M. Bailey David M. Bailey Ainara Cortés-Avizanda See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/icwdm_usdanwrc Part of the Natural Resources and Conservation Commons, Natural Resources Management and Policy Commons, Other Environmental Sciences Commons, Other Veterinary Medicine Commons, Population Biology Commons, Terrestrial and Aquatic Ecology Commons, Veterinary Infectious Diseases Commons, Veterinary Microbiology and Immunobiology Commons, Veterinary Preventive Medicine, Epidemiology, and Public Health Commons, and the Zoology Commons This Article is brought to you for free and open access by the U.S. Department of Agriculture: Animal and Plant Health Inspection Service at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USDA National Wildlife Research Center - Staff Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Marcos Moleón, Nuria Selva, David M. Bailey, David M. Bailey, Ainara Cortés-Avizanda, and Travis L. DeVault U.S. Department of Agriculture U.S. Government Publication Animal and Plant Health Inspection Service Wildlife Services Carrion Availability in Space and Time Marcos Moleón, Nuria Selva, Maria Martina Quaggiotto, David M. Bailey, Ainara Cortés-Avizanda, and Travis L. DeVault Contents Introduction 24 Causes of Carrion Production 24 Estimates of Carrion Production 25 Overall 25 Per Mortality Cause 27 Carrion Production in Relation to Species and Individuals 28 Factors Modulating Carrion Availability and Quality 29 Spatial Variation in Carrion Availability 31 Terrestrial Ecosystems 32 Aquatic Ecosystems 33 Temporal Variation in Carrion Availability 34 Terrestrial Ecosystems 34 Aquatic Ecosystems 35 Carrion Exchange at the Terrestrial-Aquatic Interface 35 Conclusions and Future Perspectives 37 References 38 M. Moleón (*) Departamento de Biología Aplicada, Universidad Miguel Hernández, Alicante, Spain Department of Conservation Biology, Doñana Biological Station (EBD-CSIC), Seville, Spain Department of Zoology, University of Granada, Granada, Spain N. Selva Institute of Nature Conservation, Polish Academy of Sciences, Kraków, Poland M. M. Quaggiotto · D. M. Bailey Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK e-mail: [email protected] A. Cortés-Avizanda Department of Conservation Biology, Doñana Biological Station (EBD-CSIC), Seville, Spain Animal Ecology and Demography Group, IMEDEA (CSIC-UIB), Palma de Mallorca, Spain T. L. DeVault US Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, Sandusky, OH, USA e-mail: [email protected] © Springer Nature Switzerland AG 2019 23 P. P. Olea et al. (eds.), Carrion Ecology and Management, Wildlife Research Monographs 2, https://doi.org/10.1007/978-3-030-16501-7_2 24 M. Moleón et al. Introduction Availability of carrion to scavengers is a central issue in carrion ecology and man- agement, and is crucial for understanding the evolution of scavenging behaviour. Compared to live animals, their carcasses are relatively unpredictable in space and time in natural conditions, with a few exceptions (see below, especially Sect. “Carrion Exchange at the Terrestrial-Aquatic Interface”). Carrion is also an ephem- eral food resource due to the action of a plethora of consumers, from microorgan- isms to large vertebrates, as well as to desiccation (i.e., loss of water content; DeVault et al. 2003; Beasley et al. 2012; Barton et al. 2013; Moleón et al. 2014). With a focus on vertebrate carcasses, here we give an overview of (a) the causes that produce carrion, (b) the rate of carrion production, (c) the factors affecting carrion quality, and (d) the distribution of carrion in space and time, both in terrestrial and aquatic environments (including their interface). In this chapter, we will focus on naturally produced carrion, whereas non-natural causes of animal mortality are described in chapter “Human-Mediated Carrion: Effects on Ecological Processes”. However, throughout this chapter we also refer to extensive livestock carrion, because in the absence of strong restrictions such as those imposed in the European Community after the bovine spongiform encephalopathy crisis (Donázar et al. 2009; Margalida et al. 2010), the spatiotemporal availability of carrion of extensive livestock and wild ungulates is similar. Causes of Carrion Production Animals commonly die from natural causes such as predation, starvation, parasites, disease, adverse climatic conditions and accidents. Many animals die naturally during the most susceptible stages of life: early when vulnerability reduces their survival, late because of senescence. Also, animals may die from casualties related to humans (see chapter “Human-Mediated Carrion: Effects on Ecological Processes”), which include intentional mortality sources such as game hunting, fisheries, deliberate poisoning and poaching, as well as unintentional mortality causes such as collisions with infrastruc- tures, road kills, ship strikes, emerging infectious diseases and environmental toxins (Burkholder et al. 1992; Harvell et al. 1999; Laist et al. 2001; Fisher et al. 2006; Lambertucci et al. 2010; Collins and Kays 2011; Koch et al. 2013; Jepson et al. 2013; Wright et al. 2013; Kühn et al. 2015; Benbow et al. 2016). Further, these causes of death often work in concert (Newton 1998). For instance, cold weather conditions may increase the requirement of energy intake and thus increase the risk of starvation (Begon et al. 2006; Conover et al. 2013). Moreover, animals weakened by disease are more prone to predation (Schaller 1972) and, in some cases, collisions with automo- biles (Møller et al. 2011). In terrestrial biomes, most vertebrates usually die due to predation and diseases. Food and water shortage are major drivers of herbivore mortality, either directly or Carrion Availability in Space and Time 25 indirectly via enhancing vulnerability to predation, pathogens and others (Pereira et al. 2014). Moreover, exhaustion suffered during long-distance migrations may increase ungulate, bat, and bird mortality rates through different mechanisms (e.g., Geluso et al. 1976; Mduma et al. 1999). Apex carnivores, in contrast, mostly die as a consequence of competition (including intraguild—both inter- and intraspecific— killing; Palomares and Caro 1999; Thompson et al. 2015), parasites, and senescence. In aquatic ecosystems, for some anadromous fish species (e.g. Pacific salmonids Onchorhynchus spp.), reproduction coincides with death. Necropsies of stranded marine mammals and turtles revealed these animals are susceptible to a wide range of parasites and viruses (Harvell et al. 1999; Arbelo et al. 2013; Work et al. 2015). Toxic diatom blooms can produce massive mortalities among sea lions (Scholin et al. 2000). Furthermore, mortality events can be also associated with large-scale climatic perturbations (Evans et al. 2005). In the South Pacific, for instance, mass mortality of Pygmy killer whales (Feresa attenuata) was linked with extreme mete- orological conditions, such as the hurricanes Marylyn and Jim (Clua et al. 2014). Furthermore, fish kills can be attributed to natural conditions of oxygen deficiency (Stachowitsch 1984), extreme cold waters (Marsh et al. 1999; Hoag 2003) or river water acidification (Fjellheim and Raddum1990 ). Similar to large animals in ter- restrial ecosystems, whales and large sharks are probably subject to reduced preda- tion risk and thus senescence and disease must be the most important natural causes of mortality, at least for adults. Estimates of Carrion Production Quantifying how much carrion is produced in ecosystems is one of the most impor- tant, although probably the most overlooked, aspect of carrion ecology (Oro et al. 2013). This is mostly due to methodological difficulties in obtaining empirical data in both terrestrial and aquatic systems. Estimating how much carrion is produced temporally and spatially is a complex issue that requires intensive fieldwork (e.g., Selva 2004), sometimes in combination with sophisticated modelling approaches (e.g., Wilmers and Getz 2004, 2005; Margalida et al. 2011). Overall In terrestrial ecosystems, as we show in Table 1, only a few studies have provided estimates of carrion biomass production per units of time and space in natural con- ditions (provision to dumps and vulture feeding stations, intensive livestock debris and game hunting remains are considered in chapter “Human-Mediated Carrion: Effects on Ecological Processes” because of their human origin). All these studies have focused on ungulates (wild, domestic or both). When all mortality causes are 26 M. Moleón et al. considered together, carrion is produced at an annual rate of up to ca. 700 kg/km2. In all cases, carrion supply ranged between tens to hundreds of kg/km2, although estimation methodologies, as well as the species evaluated, were highly heteroge- neous among the reviewed studies (Table 1). In well-preserved coastal systems, carcass supply can be substantially higher than inland. On the